Journal of Zoology
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Journal of Zoology. Print ISSN 0952-8369
Stable isotopes of oxygen reveal dispersal patterns of the
South American sea lion in the southwestern Atlantic
Ocean
L. Zenteno1, E. Crespo2,3, N. Goodall4,5, A. Aguilar1, L. de Oliveira6, M. Drago1, E. R. Secchi7, N. Garcia2,3
& L. Cardona1
1 Department of Animal Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain
2 Laboratory of Marine Mammals, Centro Nacional Patagónico (CENPAT-CONICET), Puerto Madryn, Argentina
3 National University of Patagonia, Puerto Madryn, Argentina
4 Museo Acatushún de Aves y Mamíferos Marinos Australes, Ushuaia, Tierra del Fuego, Argentina
5 Centro Austral de Investigaciones Científicas (CADIC), Ushuaia, Tierra del Fuego, Argentina
6 Study Group of Aquatic Mammals of Rio Grande do Sul (GEMARS), Porto Alegre, RS, Brazil
7 Laboratório de Ecologia e Conservação da Megafauna Marinha, Instituto de Oceanografia, Universidade Federal do Rio Grande (FURG), Río Grande,
RS, Brazil
Keywords
bone; bioapatite; oxygen isotopes; dispersal
patterns; habitat; pinnipeds.
Correspondence
Lisette Zenteno, Department of Animal
Biology, University of Barcelona, Av.
Diagonal, 643, 08028 Barcelona, Spain
Email: [email protected]
Editor: Virginia Hayssen
Received 31 October 2012; revised 23 May
2013; accepted 30 May 2013
doi:10.1111/jzo.12051
Abstract
Stable isotopes of oxygen have been widely used to reconstruct paleotemperatures
and to investigate the thermal environment of fishes and mollusks, but they have
only occasionally been used as geographical markers in marine systems. As bone
apatite grows at a constant temperature in marine mammals and food is the major
source of water for these animals, particularly for pinnipeds, variations in the ratio
of stable isotopes of oxygen (d18O) of bone apatite will likely reflect changes in the
d18O values of diet, and thus of the surrounding water mass, despite the potential
confounding role of factors as the proximate composition of diet, sex and body
size. Here, we used the d18O values in bone apatite to investigate whether adult
males of South American sea lion (Otaria byronia), from three regions in southwestern Atlantic Ocean (Brazil, Patagonia and Tierra del Fuego in Argentina),
used the same water masses to forage and whether differences exist in the water
masses used by sea lions differing according to sex and developmental stage.
Statistically significant differences were observed among the d18O bone values of
adult males from the three regions, with those from Patagonia more enriched in
18
O, as expected from the d18Oseawater values. These results revealed restricted dispersal movements of adult males between the three areas. On the other hand, adult
males and females from Patagonia did not differ in average d18Obone values, thus
indicating the use of foraging grounds within the same water mass. Finally, the
variability in the d18Obone values of young of both sexes was much wider than the
adults of the same sex from the same region, which suggests the existence of a
juvenile dispersal phase in both sexes, although much shorter in females than in
males. These results confirm the usefulness of stable isotopes of oxygen as habitats
tracers in marine mammals.
Introduction
Recent advances in satellite telemetry have helped to fill the
gap in our knowledge of animal movements, but these
methods are expensive and tracking is often restricted to a few
individuals for relatively short periods (Shillinger et al., 2008).
Biogeochemical markers such as stable isotopes lack the
detailed resolution of satellite tags, but laboratory analyses
are inexpensive and provide information integrated over
known and predictable timescales that can be linked directly
Journal of Zoology 291 (2013) 119–126 © 2013 The Zoological Society of London
to geographical regions if the isotopic landscape, or isoscape,
has been previously reconstructed (Hobson & Wassenaar,
2008; Graham et al., 2010).
Stable isotopes are known from several chemical elements
and the relative abundance of two stable isotopes in a sample
is usually expressed as a ratio between the heavy and the light
isotope and compared with that ratio in a standard (Hobson
& Wassenaar, 2008). Stable isotopes of carbon and nitrogen
are among the most widely used biogeochemical markers in
ecological studies (Koch, 2008) and maps describing the vari119
Oxygen isotopes reveal sea lion dispersal patterns
ability of their stable isotope ratios across entire oceans are
available (Graham et al., 2010). However, interpreting
changes in d13C and d15N values to track migrations is possible
only if no major dietary shifts occur during migrations, which
is not necessarily true for opportunistic predators.
Stable isotopes of oxygen have been widely used to reconstruct paleotemperatures (e.g. Schöne et al., 2004) and to
investigate the thermal environment of fishes (e.g. Jones &
Campana, 2009) and mollusks (e.g. Soldati et al., 2009),
because carbonates in biominerals become enriched in 18O as
temperature declines (Kim & O’Neil, 1997; Soldati et al.,
2009). Nevertheless, most of the current variability in the
ratios of stable isotopes of oxygen in the ocean is not linked to
thermal gradients, but caused by the preferential evaporation
of the light isotope and the preferential condensation of the
heavy isotope (Bowen, 2010). Accordingly, a sharp contrast
exists between d18O values in freshwater and seawater and
well-defined latitudinal gradients of d18O values also exist
from mid to high latitudes in most oceans (Bowen, 2010).
Such regularities make stable isotopes of oxygen potential
habitats tracers for marine species moving between marine
and freshwater ecosystems and for species with distribution
ranges spanning over marine regions differing in d18O values.
However, stable oxygen isotopes have seldom been used to
track the migrations of marine vertebrates (e.g. Yoshida &
Miyazaki, 1991; Clementz & Koch, 2001; Coulson et al., 2008;
Ramos, González-Solís & Ruiz, 2009). A constant body temperature does not pose any actual limitation to the use of
stable isotopes as tracers in marine mammal, as the d18O
values of endotherms records dietary information and not
body temperature (Koch, Fogel & Tuross, 1994; Bryant &
Froelich, 1995; Kohn, 1996; Koch, 2008). Therefore, d18O
values can be a useful tracer for investigating marine mammal
habitats in areas where well-defined gradients exist.
South American sea lions, Otaria byronia, are widely distributed along both coasts of South America (Vaz-Ferreira,
1982). Genetic markers suggest female philopatry and malemediated gene flow among populations in the southwestern
South Atlantic Ocean (Szapkievich et al., 1999; Freilich, 2004;
Túnez et al., 2007, 2010; Artico et al., 2010 and Feijoo et al.,
2011). Tagging confirmed that young females often remain
close to their breeding site (Thompson et al., 1998; Campagna
et al., 2001), whereas adult males travel longer distances than
females after the breeding season (Vaz-Ferreira, 1982; Rosas
et al., 1994; Giardino et al., 2009). Nevertheless, nothing is
known about the actual duration of the juvenile dispersal
phase or the actual fidelity of adults to a particular stretch of
coastline.
Stable oxygen isotopes could provide an insight into these
issues because the d18Oseawater values of Patagonia are higher
than those from southern Brazil and Tierra del Fuego (Bowen,
2010). Accordingly, the d18Obone values in sea lions from those
three regions should not reproduce the local pattern reported
above for d18Osewater values if sea lions dispersed over scales of
more than 1000 km along the coastline of the southwestern
Atlantic Ocean. Furthermore, the d18Obone values in males and
females from the same region would differ if males had larger
dispersal areas than females along the coastline. Finally,
120
L. Zenteno et al.
d18Obone values would be similar across age classes of female
sea lions from the same region if young females remained close
to their natal site, but they would vary across age classes of
male sea lions if young males dispersed longer distances from
their natal sites before settlement as adults. This paper
describes the variability of d18Obone values in South American
sea lions to test the three former hypotheses.
Material and methods
Sample collection
A total of 112 bone samples were collected from the skulls of
sea lions found dead between 1978 and 2010 in three coastal
zones of the southwestern South Atlantic coast of South
America. Samples from southern Brazil (from 29°S to 31°S)
came from the collection from the Grupo de Estudos de
Mamíferos Aquáticos do Rio Grande do Sul at Imbé, Brazil
(17 adult males). Samples from central and northern Patagonia coasts (from 40°S to 47°S) (here after Patagonia) came
from the collection from the Centro Nacional Patagónico at
Puerto Madryn, Argentina (39 males and 39 females covering
all the developmental stages). Finally, samples from Tierra del
Fuego (from 53°S to 54°S) were obtained from the collection
from the Museo Acatushún de Aves y Mamíferos Marinos
Australes, near at Ushuaia, Argentina (17 adult males). These
three regions differed in salinity levels (Fig. 1a) and d18Oseawater
gradients (Fig. 1b).
Age, sex and development stage
determination
Sea lions obtained from these collections had previously been
aged by counting growth layers in the dentine of the canines
(after being decalcified in 5% formic or nitric acid and thick
sections stained with hematoxylin (Crespo, 1988). Sex was
assessed according to secondary sex characteristics at the time
of collection and measurements of the skull (Crespo, 1988).
The life span of sea lions is around 20 years (Crespo, 1988),
with females reaching adulthood at about 4 years of age and
males mating for the first time when they are at least 9 years
old (Grandi et al., 2010). Based on these data, we established
four developmental stages; young post-weaned and not yet
sexually mature individuals between 1 and 5 years of age for
males and between 1 and 3 years of age for females; early adult
sexually mature individuals between 7 and 8 years of age for
males and between 5 and 7 years of age for females; adult
sexually mature individuals between 9 and 12 years of age for
males and between 8 and 12 years of age for females and senile
sexually mature individuals >13 years old for males and >12
years old for females. The main difference between early
adults and adults is that the former can still grow in length,
whereas the latter are thought to have ceased length growth.
Sample preparation
Each skull sample used for the isotopic analysis consisted of a
fragment of turbinate bone from the nasal cavity, which was
Journal of Zoology 291 (2013) 119–126 © 2013 The Zoological Society of London
L. Zenteno et al.
Oxygen isotopes reveal sea lion dispersal patterns
30°S
BRAZIL
URUGUAY
BRAZIL
URUGUAY
B
ARGENTINA
B
ARGENTINA
40°S
Surface salinity (psu)
P
P
30
27.3
28.4
35
50°S
d18O (SMOW)
TF
TF
100Km
60°W
100Km
50°W
60°W
50°W
Figure 1 Map of southern South America, showing the study areas (B, southern Brazil; P, central and northern Patagonia; TF, Tierra del Fuego), sea
surface salinity [left panel, according to Falabella et al. (2009)] and d18Oseawater values (right panel, according to Bowen, 2010).
ground with a mortar and pestle. Approximately 15 mg of
sample powder were soaked with 30% hydrogen peroxide
solution for 24 h, rinsed five times with deionized water,
soaked for another 24 h in a solution of acetic acid (1M)
buffered to pH~ 4.5 with 1M calcium acetate, rinsed again five
times with deionized water and finally dried for 24 h (Koch,
Tuross & Fogel, 1997).
Stable isotope analyses
Samples were analyzed for oxygen isotope ratios via a Carbonate Kiel Device III carbonate preparation system (Thermo
Electron – Dual Inlet, Thermo Finnigan, Bremen, Germany)
linked to a gas source mass spectrometer in the ScientificTechnical Services at the University of Barcelona. Approximately, 1.0 mg of bone powder was dissolved in 100%
phosphoric acid at 70°C with concurrent cryogenic trapping
of CO2 and H2O. The CO2 was then admitted to the mass
spectrometer for analysis. The measured isotope compositions
were normalized to the NBS 19 calcite standard, with a value
of d18O = -2.20‰ relative to Vienna Pee Dee Belemnite
(VPDB). Precision of replicate analyses for d18O was ⫾0.06‰
[standard deviation (sd)]. As d18O values in zoology are more
commonly presented relative to Vienna Standard Mean Ocean
Water (VSMOW), d18O values were converted from VPDB to
VSMOW using the formula d18O (VSMOW) = [d18O (VPDB)
¥ 1.03086] + 30.86 (Koch et al., 1997). The stable isotope
abundances are expressed in delta (d) notation in parts per
thousand (‰), using the formula d18O = [(18O/16Osample ⫼ 18O/
16
Ostandard -1) ¥ 1.000], where the standard is VSMOW.
Journal of Zoology 291 (2013) 119–126 © 2013 The Zoological Society of London
Data analyses
Data are presented as mean ⫾ sd, unless otherwise stated.
Normality was tested with the Lilleford test and homogeneity
of variances with the Levene test. The Kruskal–Wallis test was
used to compare the d18Obone values of males from southern
Brazil, Patagonia and Tierra del Fuego because the three datasets were heteroskedastic (Levene test, W2.48 = 7.280, P = 0.02).
The Kruskal–Wallis test was followed by a post hoc nonparametric multiple comparisons test. The Student t-test was used
to compare d18Obone values of males and females from Patagonia and the Pearson regression analysis was used to test the
hypothesis that d18Obone values remained stable after adulthood. Significance was tested at a = 0.05. All statistical analyses were performed with PASW Statistics (Version 17.0 for
Windows, SPSS, version 17.0, Spain), except the nonparametric multiple comparison test, performed following Zar (1984).
Results
The bone of male South American sea lions from Patagonia
was significantly enriched in 18O when compared with that of
males from southern Brazil and Tierra del Fuego (Fig. 2;
Kruskal–Wallis test, chi-square = 6.210, d.f. = 2, P = 0.045 n =
17 for each region). Post hoc pairwise comparisons of the
mean bone d18O values between regions revealed statistically
significant differences between Brazil and Patagonia (q =
4.295, P = 0.002) and marginally significant differences
between Patagonia and Tierra del Fuego (q = 3.193, P =
0.070), whereas differences between Brazil and Tierra del
121
Oxygen isotopes reveal sea lion dispersal patterns
L. Zenteno et al.
30
31
(a)
30
d18O (SMOW ‰)
d18O (SMOW ‰)
29
28
29
28
Min-Max
25%-75%
Median value
Outliers
27
27
Min-Max
25%-75%
Median value
Outliers
26
Young
n:10
S Brazil
N-C Patagonia
Tierra del Fuego
n:17
n:17
n:17
(b)
30
d18O (SMOW ‰)
d18O (SMOW ‰)
Senile
n:9
29
28
27
29
26
Young
n:10
28
Early adult
n:9
Adult
n:10
Senile
n:10
Figure 4 Boxplots of the d18O values in the bone of four developmental
stages of South American sea lions, Otaria byronia, found dead in
central and northern Patagonia. (a) Males; (b) Females.
Min-Max
25%-75%
Median value
Males
Females
n:19
n:20
Figure 3 Boxplots of the d O values in the bone of adult males and
females South American sea lions, Otaria byronia, found dead in central
and northern Patagonia.
18
Fuego were not statistically significant (q = 0.490, P > 0.500).
These differences suggested limited exchange of individuals
among the three regions.
Adult male and female sea lions from Patagonia did not
differ in d18Obone values (Fig. 3; t = 0.861, d.f. = 37, P = 0.395),
indicating that they potentially used the same water masses for
foraging. On the other hand, young animals of both sexes
exhibited a much larger variability in d18Obone values in comparison with the adults of the same sex (Fig. 4), as demonstrated by heteroskedasticity both among male (Levene test;
122
Adult
n:10
31
Figure 2 Boxplots of the d18O values in the bone of male South American sea lions, Otaria byronia, found dead on beaches in three regions
along the coastline of the southwestern South Atlantic Ocean.
30
Early adult
n:10
males: W3.35 = 4.523, P = 0.009) and female developmental
stages (Levene test; W3.35 = 3.145, P = 0.037). The variability of
the d18Obone values of females decreased sharply at first maturity but remained high in males for several years after sexual
maturity. Finally, after first maturity, a statistically significant
though moderate decrease in the d18Obone values occurred
in females with age (r2 = 0.319, P = 0.001), but not in males
(P = 0.946).
Discussion
Previous studies using external tags have concluded that adult
male South American sea lions may travel longer distances
than females after the breeding season (Vaz-Ferreira, 1982;
Rosas et al., 1994; Giardino et al., 2009) and may also exhibit
a high degree of fidelity to haul-out sites on consecutive
nonbreeding seasons (Giardino et al., 2009). Nevertheless,
Journal of Zoology 291 (2013) 119–126 © 2013 The Zoological Society of London
L. Zenteno et al.
external tags do not last for a long time on sea lions (e.g.
Oliveira, 2010) and resightings a few months after tagging are
scarce (Giardino et al., 2009). Similarly, satellite tags remain
attached to sea lions for only a few months and have offered
no information about interannual movements (Campagna
et al., 2001; Riet-Sapriza et al., 2012). As a consequence, the
actual proportion of adult males moving to distant foraging
grounds after the breeding season has remained unknown.
Stable isotope analysis offers an alternative approach,
although a number of confounding factors should be considered. Firstly, bone samples come from dead stranded sea lions,
which are likely biased for sex ratio and age distribution.
However, such biases are not relevant for the hypothesis here
to be tested because comparisons among areas were based
only on adult males. Furthermore, recent research on dead
stranded marine mammals and sea turtles has revealed that
decomposition does not significantly modify the stable isotope
ratios of soft tissues (Payo Payo et al., 2013) and hence is not
expected to have any impact on the d18O values of biominerals.
The existence of a second set of potential confounding
factors is suggested by the water balance models developed for
other mammals (Kohn, 1996; O’Grady et al., 2012; Podlesak
et al., 2012). Sea lions obtain the water they need from food
(Ortiz, 2001; Berta, Sumich & Kovacs, 2005). South American
sea lions consume a diversity of prey species, differing widely
in water and fat contents, but not in protein contents (Drago
et al., 2009b, 2010). Therefore, dietary changes between sexes
and age classes (Drago et al., 2009a) may result in differences
in the relative contribution of metabolic and preformed water
to the water supply of sea lions. As the metabolic water generated by food oxidation is 18O-enriched relative to ingested
water and preformed water in the diet (Newsome, Clementz &
Koch, 2010) and the consumption of fat-rich prey declines
with body size in sea lions (Drago et al., 2009a), younger
developmental stages and females might be more enriched in
18
O than older age classes and males, even if they forage in the
same water mass.
Reproduction is another potentially confounding factor,
not only because lactation results in a high water turnover rate
in adult females, but also because male and females differ
dramatically in haul-out time and foraging behavior during
the breeding season. Adult male sea lions spend as much as 40
days in the beach during the reproductive season (Campagna,
1985) and they fast during that time (Campagna et al., 2001).
Conversely, females resume feeding as soon as they have been
fertilized by males (Campagna & Leboeuf, 1988) and alternate
foraging bouts with periods on the beach nursing pups
(Campagna et al., 2001). Fasting animals rely primarily on the
metabolism of fat, and secondarily on protein, to maintain
their water balance (Worthy & Lavigne, 1982), and hence
fasting for long periods is expected to increase the d18O values
of body water. Furthermore, males are exposed to high air
temperatures during the breeding season, at least in Uruguay
and northern Patagonia, which likely increase water loss
through sweating (Khamas et al., 2012).
Despite all these potential sources of variability, the
absence of statistically significant differences in the average
d18Obone values across sexes and developmental stages in the
Journal of Zoology 291 (2013) 119–126 © 2013 The Zoological Society of London
Oxygen isotopes reveal sea lion dispersal patterns
sea lions from Patagonia suggest that these factors considered
are actually minor sources of variability. Alternatively, diet
might not vary across sexes and developmental stages, but this
is unlikely considering the dietary information published to
date (Koen-Alonso et al., 2000; Drago et al., 2009b). Hence,
the regional variability in the d18Oseawater values stands as the
most likely source of variability for the differences observed
among males from Brazil, Patagonia and Tierra del Fuego. If
so, the results reported here suggest that adult males are quite
faithful to a particular coastal region for at least several years
because the latitudinal differences observed in the d18Obone
values of males were in agreement with the latitudinal patterns
of salinity (Guerrero & Piola, 1997) and d18O sea water values in
the region (Bowen, 2010). In addition, the rate of turnover
of oxygen isotopes in hydroxyapatite is assumed to
represent several years in large adult mammals (Schwarcz &
Schoeninger, 1991; Ambrose & Norr, 1993).
Furthermore, the sd of the d18Obone values in males was low
in Brazil (⫾0.32‰) and Patagonia (⫾0.26‰), but much
higher in Tierra del Fuego (⫾0.67‰). When these figures are
compared with the d18Oseawater gradients in each region (0.28‰
every 100 km from Rio de Janeiro to Rio de la Plata, 0.11‰
every 100 km from Rio de la Plata to central Patagonia and
0.08‰ every 100 km from central Patagonia to Tierra del
Fuego; http://data.giss.nasa.gov/o18data/), males stranding in
southern Brazil had foraged along approximately 230 km of
coastline, those from Patagonia over 470 km of coastline and
those from Tierra del Fuego over 1700 km of coastline (sd of
d18Obone = ⫾0.67‰). Nevertheless, the high sd observed in
Tierra del Fuego could be caused by a high degree of individual variability in the use of the relatively diluted channels
of the Fuegian Archipelago and the saltier Atlantic waters
(Guerrero & Piola, 1997).
Conversely, the absence of differences in the average
d18Obone values of adult males and females from Patagonia
suggests that they share the same water mass year round, a
conclusion that cannot be extrapolated to southern Brazil and
Tierra del Fuego because only adult males were analyzed there
due to the scarcity of female skulls in the museum collections
from those areas. The scarcity of females for southern Brazil is
because of the rarity of females in the local haul-out sites
(Rosas et al., 1994), but this is not true for Tierra del Fuego
(Schiavini, Crespo & Szapkievich, 2004).
It should be noted that sharing a water mass does not
necessarily means using the same foraging grounds, because
the values of d18Oseawater vary with latitude but not longitude
over the continental shelf of southwestern South America
(Bowen, 2010). Hence, animals using foraging grounds at a
different distance from the coastline but at the same latitude
will not differ in their d18Obone values, which explain why adult
male and female from Patagonia have similar d18Obone values
although females forage in more coastal areas than males
(Campagna et al., 2001).
In contrast, the average d18Obone values of young specimens
of both sexes collected in northern Patagonia did not differ
either from those of the adult and senile individuals, but were
more variable. This was also true for early adult males, but
not for early adult females. Although the d18Obone values of
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Oxygen isotopes reveal sea lion dispersal patterns
young specimens integrate the values of hydroxyapatite after
weaning with those deposited in uterus and during lactation,
the latter signals decays after weaning and vanish totally after
several months (Newsome et al., 2010).The high variability
observed in the d18Obone values of juveniles reveals the presence
in the same region of individuals with contrasting foraging
histories during the years previous to death which for young
specimens could result from differences in age and the persistence of the pre-weaning signals in the youngest animals. This
is because suckling mammals are expected to be enriched
in the heavier isotopes as compared with their mothers;
however, suckling signal decays after weaning (Newsome
et al., 2010). Although this pattern is well established for
nitrogen (Newsome et al., 2010) and some of the young individuals analyzed here were young enough to exhibit traces of
the suckling signal in their nitrogen stable isotope ratios
(Drago et al., 2009a), experimental evidence supporting the
existence of a suckling signal for oxygen stable isotope ratios
in bone is ambiguous (Williams, White & Longstaffe, 2005;
Kirsanow & Tuross, 2011). However, no trace of the suckling
signal is expected to remain in early adult males (Drago et al.,
2009a) and hence the high sd observed in that group, when
compared with that of older males, should have a different
explanation.
Actually, the range of d18Obone values observed in young
specimens of both sexes and in early adult males greatly overlapped with the range of d18Obone values reported for adult
males across the study area, which suggests that young specimens of both sexes disperse before settlement along most of
the range of the species in the southwestern Atlantic Ocean,
from Uruguay to Tierra del Fuego. This is in sharp contrast
with the dispersal pattern of young Steller sea lions (Eumetopias jubatus) in the North Pacific, where only males conducted
long distance (>500 km) movements, although the range of
round trip distance of juveniles increases with age in both
sexes (Raum-Suryan et al., 2004).
Genetic markers suggested philopatry for females, but not
for males, which will disperse over much larger ranges and will
be responsible for gene flow (Szapkievich et al., 1999; Freilich,
2004; Túnez et al., 2007, 2010; Artico et al., 2010 and Feijoo
et al., 2011). The sudden decreases in the variability of the
d18Obone values of females observed after adulthood cannot be
explained by bone remodeling (Schwarcz & Schoeninger,
1991; Ambrose & Norr, 1993) and suggest that females come
back to their natal regions for settlement. Conversely, the sd
of the d18Obone values of males decreases more slowly as they
grow older at a rate consistent with the expected apatite turnover, suggesting that males do not necessarily come back to
their natal areas for settlement. Comparing the sd of d18Obone
values observed in young male sea lions from Patagonia
(⫾0.81‰) and the gradient of d18Oseawater values above
reported for that region suggests that young males originated
from a 2000 km stretch of coastline. Nevertheless, the duration of the juvenile dispersal phase is much longer in males (8
years) than in females (3 years), as suggested by the sudden
decline of the variability of the d18Obone after adulthood in
females but not in males. Therefore, the overall evidence indicates that both males and females may disperse over long
124
L. Zenteno et al.
distances as juveniles, but females do not settle far from their
natal region although males can, as previously reported for
other pinnipeds (e.g. Burg, Trites & Smith, 1999; Hoffman
et al., 2006; González-Suárez et al., 2009).
In conclusion, the results are consistent with information
from genetic markers indicating population isolation by distance and male-mediated gene flow, but suggest that once they
become reproductively active, early adult males settling far
away from their natal rookeries are the ones responsible for
gene flow. Furthermore, these results demonstrate that stable
isotopes of oxygen represent a useful and inexpensive
approach to the study habitat use and dispersal patterns in
marine mammals, and particularly highlight the importance
of the bone material deposited in museums and other scientific
collections as a source of samples.
Acknowledgments
Thanks to the staff of the Marine Mammal Laboratory of the
Centro Nacional Patagónico (CENPAT-CONICET) for the
fieldwork and for the age assessment of the sampled individuals. R.N.P. Goodall is grateful for grants for beach surveys
from the Committee for Research and Exploration (CRE) of
the National Geographic Society. We also thank at the Centro
Austral de Investigaciones Científicas (CADIC-CONICET)
for access to their collections. The Comisión Nacional de
Investigación Científica y Tecnológica (CONICYT) of Chile
supported L.Z. through a PhD fellowship. This research was
funded by the Fundación BBVA through the project ‘Efectos
de la explotación humana sobre depredadores apicales y la
estructura de la red trófica del Mar Argentino durante los
últimos 6000 años’ (BIOCON08-194/09 2009-2011) and
Agencia Nacional de Promoción Científica y Tecnológica
(PICT N° 2110). The ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq’ (Brazil) provided
scholarships to E.R. Secchi (PQ 307843/2011-4). A previous
version of this paper benefited from the comments by Dr.
Luciano Valenzuela and another anonymous reviewer.
References
Ambrose, S.H. & Norr, L. (1993). Experimental evidence for
the relationship of the carbon isotope ratios of whole diet
and dietary protein to those of bone collagen and carbonate. In Prehistoric human bone-archaeology at the molecular
level: 1–37. Lambert, J.B. & Grupe, G. (Eds). Berlin:
Springer-Verlag.
Artico, L.O., Bianchini, A., Grubel, K.S., Monteiro, D.S.,
Estima, S.C., de Oliveira, L.R., Bonatto, S.L. & Marins,
L.F. (2010). Mitochondrial control region haplotypes of the
South American sea lion Otaria flavescens (Shaw, 1800).
Braz. J. Med. Biol. Res. 43, 816–820.
Berta, A., Sumich, J.S. & Kovacs, K.M. (2005). Marine
mammals, an evolutionary approach. 2nd edn. New York:
Academic Press.
Bowen, G.J. (2010). Isoscapes: spatial pattern in isotopic biogeochemistry. Annu. Rev. Earth Planet. Sci. 38, 161–187.
Journal of Zoology 291 (2013) 119–126 © 2013 The Zoological Society of London
L. Zenteno et al.
Bryant, J.D. & Froelich, P.N. (1995). A model of oxygen
isotope fractionation in body water of large mammals.
Geochim. Cosmochim. Acta 59, 4523–4537.
Burg, T.M., Trites, A.W. & Smith, M.J. (1999). Mitochondrial and microsatellite DNA analyses of harbour seal
population structure in the northeast Pacific Ocean. Can. J.
Zool. 77, 930–943.
Campagna, C. (1985). The breeding cycle of the southern sea
lion, Otaria byronia. Mar. Mamm. Sci. 1, 210–218.
Campagna, C. & LeBoeuf, B. (1988). Reproductive behavior
of southern sea lions. Behaviour 104, 233–261.
Campagna, C., Werner, R., Karesh, W., Marin, M.R.,
Koontz, F., Cook, R. & Koontz, C. (2001). Movements
and location at sea of South American sea lions (Otaria
flavescens). J. Zool. (Lond.) 257, 205–220.
Clementz, M.T. & Koch, P.L. (2001). Differentiating aquatic
mammal habitat and foraging ecology with stable isotopes
in tooth enamel. Oecologia 129, 461–472.
Coulson, A.B., Kohn, M.J., Shirley, M.H., Joyce, W.G. &
Barrick, R.E. (2008). Phosphate oxygen isotopes from
marine turtle bones: ecologic and paleoclimatic applications. Palaeogeogr. Palaeoclimatol. Palaeoecol. 264, 78–84.
Crespo, E.A. (1988). Dinámica poblacional del lobo marino de
un pelo Otaria flavescens (Shaw, 1800), en el norte del
Litoral Patagónico. PhD thesis, Universidad Nacional de
Buenos Aires.
Drago, M., Cardona, L., Aguilar, A., Crespo, E.A., Ameghino, S. & García, N. (2010). Diet of lactating South
American sea lions, as inferred from stable isotopes, influences pup growth. Mar. Mamm. Sci. 26, 309–323.
Drago, M., Cardona, L., Crespo, E.A. & Aguilar, A. (2009a).
Ontogenic dietary changes in South American sea lions. J.
Zool. (Lond.) 279, 251–261.
Drago, M., Crespo, E.A., Aguilar, A., Cardona, L., García,
N., Dans, S.L. & Goodall, N. (2009b). Historic diet change
of the South American sea lion in Patagonia as revealed by
isotopic analysis. Mar. Ecol. Prog. Ser. 384, 273–286.
Falabella, V., Campagna, C. & Croxall, J. (2009). Atlas del
Mar Patagónico. Wildlife Conservation Society and Birdlife
International, Buenos Aires.
Feijoo, M., Lessa, E.P., Loizaga de Castro, R. & Crespo,
E.A. (2011). Mitochondrial and microsatellite assessment of
population structure of South American sea lion (Otaria
flavescens) in the Southwestern Atlantic Ocean. Mar. Biol.
158, 1857–1867.
Freilich, S.Y. (2004). Genetic diversity and population genetic
structure in the South American Sea Lion (Otaria flavescens) from Argentina and the Falkland Islands. PhD thesis,
University of Durham, UK.
Giardino, G., Mandiola, M.A., Bastida, R. & Rodríguez, D.
(2009). Movimientos estivales de machos de Otaria flavescens entre Puerto Quequén (Argentina), Uruguay y Patagonia. In Report to workshop on the status of South American
sea lions along the distribution range. Crespo, E. A., Oliva,
D., Dans, S.L. & Sepúlveda, M. Valparaíso, Chile.
Journal of Zoology 291 (2013) 119–126 © 2013 The Zoological Society of London
Oxygen isotopes reveal sea lion dispersal patterns
González-Suárez, M., Flatz, R., Aurioles-Gamboa, D.,
Hedrick, P.W. & Gerber, L.R. (2009). Isolation by distance
among California sea lion populations in Mexico: redefining management stocks. Mol. Ecol. 18, 1088–1099.
Graham, B.S., Koch, P.L., Newsome, S.D., McMahon, K.W.
& Aurioles, D. (2010). Using isoscapes to trace the movements and foraging behavior of top predators in oceanic
ecosystems. In Isoscapes: understanding movement, pattern
and process on earth through isotope mapping: 299–318.
West, J.B., Bowen, G.J., Dawson, T.E. & Tu, K.P. (Eds).
New York: Springer.
Grandi, M.F., Dans, S.L., García, N.E. & Crespo, E.A.
(2010). Growth and age at sexual maturity of South American sea lions. Mamm. Biol. 75, 427–436.
Guerrero, R.A. & Piola, A.R. (1997). Masas de agua en la
plataforma continental. In El mar argentino y sus recursos
pesqueros; Antecedentes históricos de las exploraciones en el
mar y las características ambientales: 107–118. Boschi, E.E.
(Ed.). Mar del Plata: Instituto Nacional de Investigación y
Desarrollo Pesquero, Secretaría de Agricultura, Ganadería,
Pesca y Alimentación.
Hobson, K.A. & Wassenaar, L.I. (2008). Tracking animal
migration with stable isotopes. 1st edn. London: Academic
Press.
Hoffman, J.I., Matson, C., Amos, W., Loughlin, T.R. &
Bickham, J.W. (2006). Deep genetic subdivision within a
continuously distributed and highly vagile marine mammal,
the Steller’s sea lion Eumetopias jubatus. Mol. Ecol. 15,
2821–2832.
Jones, J.B. & Campana, S.E. (2009). Stable oxygen isotope
reconstruction of ambient temperature during the collapse
of a cod (Gadus morhua) fishery. Ecol. Appl. 19, 1500–1514.
Khamas, W.A., Smodlaka, H., Leach-Robinson, J. & Palmer,
L. (2012). Skin histology and its role in heat dissipation in
three pinniped species. Acta Vet. Scand. 54, 1–46.
Kim, S.T. & O’Neil, J.R. (1997). Equilibrium and nonequilibrium oxygen isotope effects in synthetic carbonates.
Geochim. Cosmochim. Acta 61, 3461–3475.
Kirsanow, K. & Tuross, N. (2011). Oxygen and hydrogen isotopes in rodent tissues: impact of diet, water and ontogeny.
Palaeogeogr. Palaeoclimatol. Palaeoecol. 310, 9–16.
Koch, P.L. (2008). Isotopic study of the biology of modern
and fossil vertebrates. In Stable isotopes in ecology and environmental science: 99–154. Michener, R. & Lajtha, K.
(Eds). Oxford: Blackwell Publishing Ltd.
Koch, P.L., Fogel, M.L. & Tuross, N. (1994). Tracing the
diets of fossil animals using stable isotopes. In Stable isotopes in ecology and environmental science: 63–92. Michener,
R. & Lajtha, K. (Eds). Oxford: Blackwell Publishing Ltd.
Koch, P.L., Tuross, N. & Fogel, M.L. (1997). The effects of
sample treatment and diagenesis on the isotopic integrity of
carbonate in biogenic hydroxyapatite. J. Archaeol. Sci. 24,
417–429.
Koen-Alonso, M., Crespo, E.A., Pedraza, S.N., García, N.A.
& Coscarella, M.A. (2000). Food habits of the South
125
Oxygen isotopes reveal sea lion dispersal patterns
American sea lion, Otaria flavescens, off Patagonia, Argentina. Fish. Bull. 98, 250–263.
Kohn, M.J. (1996). Predicting animal d18O: accounting for
diet and physiological adaptation. Geochim. Cosmochim.
Acta 60, 4811–4829.
Newsome, S.D., Clementz, M.T. & Koch, P.L. (2010). Using
stable isotope biogeochemistry to study marine mammal
ecology. Mar. Mamm. Sci. 26, 509–572.
O’Grady, S.P., Valenzuela, L.O., Remien, C.H., Enright,
L.E., Jorgensen, M.J., Kaplan, J., Wagner, J., Cerling, T.E.
& Ehleringer, J.R. (2012). Hydrogen and oxygen isotope
ratios in body water and hair: modeling isotope dynamics
in nonhuman primates. Am. J. Primatol. 74, 651–660.
Oliveira, L.R. (2010). Marcação individual de pinípedes. In
Técnicas de estudos aplicadas aos mamíferos solvestres brasileiros: 137–150. Reis, N.R., Peracchi, A.L., Rossaneis,
B.K. & Fregonezi, M.N. (Org). (Eds). 1st edn. Rio de
Janeiro: Technical Books.
Ortiz, R. (2001). Osmoregulation in marine mammals. J. Exp.
Biol. 204, 1831–1844.
Payo Payo, A., Ruiz, B., Cardona, L. & Borrell, A. (2013).
Effect of tissue decomposition on stable isotope signatures
of striped dolphins Stenella coeruleoalba and loggerhead sea
turtles Caretta caretta. Aquat. Biol. 18, 141–147.
Podlesak, D.W., Bowen, G.J., O’Grady, S., Cerling, T.E. &
Ehleringer, J.R. (2012). d2H and d18O of human body
water: a GIS model to distinguish residents from nonresidents in the contiguous USA. Isotopes Environ. Health
Stud. 48, 259–279.
Ramos, R., González-Solís, J. & Ruiz, X. (2009). Linking isotopic and migratory patterns in a pelagic seabird. Oecologia
160, 97–105.
Raum-Suryan, K.L., Rehberg, M.J., Pendleton, G.W.,
Pitcher, K. & Gelatt, T.S. (2004). Development of dispersal, movement patterns, and haul-out use by pup and juvenile Steller sea lions (Eumetopias jubatus) in Alaska. Mar.
Mamm. Sci. 20, 823–850.
Riet-Sapriza, F.G., Costa, D.P., Franto-Trecu, V., Marín, Y.,
Chocca, J., González, B., Beathyate, G., Chilvers, B.L. &
Hückstadt, L.A. (2012). Foraging behaviour of lactating
South American sea lions (Otaria flavescens) and spatialtemporal resource overlap with the Uruguayan fisheries.
Deep Sea Res. II 88, 106–119.
Rosas, F.C., Pinedo, M.C., Marmontel, M. & Haimovici, M.
(1994). Seasonal movements of the South American sea
lion (Otaria flavescens, Shaw) off the Rio Grande do Sul
coast, Brazil. Mammalia 58, 51–59.
Schiavini, A.C.M., Crespo, E.A. & Szapkievich, V. (2004).
Status of the population of South American sea lion
(Otaria flavescens Shaw, 1800) in southern Argentina.
Mamm. Biol. 69, 108–118.
126
L. Zenteno et al.
Schöne, B.R., Freyre Castro, A.D., Fiebig, J., Houk, S.D.,
Oschmann, W. & Kröncke, I. (2004). Sea surface water
temperatures over the period 1884–1983 reconstructed from
oxygen isotope ratios of a bivalve mollusk shell (Arctica
islandica, southern North Sea). Palaeogeogr. Palaeoclimatol. Palaeoecol. 212, 215–232.
Schwarcz, H.P. & Schoeninger, M.J. (1991). Stable isotope
analyses in human nutritional ecology. Yearb. Phys.
Anthropol. 34, 283–321.
Shillinger, G.L., Palacios, D.M., Bailey, H., Bograd, S.J.,
Swithenbank, A.M., Gaspar, P., Wallace, B.P., Spotila,
J.R., Paladino, F.V., Piedra, R., Eckert, S.A. & Block,
B.A. (2008). Persistent leatherback turtle migrations
present opportunities for conservation. PLoS Biol. 6,
1408–1416.
Soldati, A.L., Jacob, D.E., Schöne, B.R., Bianchi, M.M. &
Hajduk, A. (2009). Seasonal periodicity of growth and
composition in valves of Diplodon chilensis patagonicus
(D’Orbigny, 1835). J. Molluscan Stud. 75, 75–85.
Szapkievich, V.B., Cappozzo, H.L., Crespo, E.A., Bernabeu,
R.O., Comas, C. & Mudry, M. (1999). Genetic relatedness
in two Southern sea lion (Otaria flavescens) rookeries in
Southwestern Atlantic. Z. Saugetierkd. 64, 1–5.
Thompson, D., Duck, C.D., McConnell, B.J. & Garrett, J.
(1998). Foraging behaviour and diet of lactating female
southern sea lions (Otaria flavescens) in the Falkland
Islands. J. Zool. (Lond.) 246, 135–146.
Túnez, J.I., Cappozzo, H.L., Nardelli, M. & Cassini, M.H.
(2010). Population genetic structure and historical
population dynamics of the South American sea lion,
Otaria flavescens, in north-central Patagonia. Genetica 138,
831–841.
Túnez, J.I., Centrón, D., Cappozzo, H.L. & Cassini, M.H.
(2007). Geographic distribution and diversity of mitochondrial DNA haplotypes in (Otaria flavescens) and fur seals
(Arctocephalus australis). Mamm. Biol. 72, 193–203.
Vaz-Ferreira, R. (1982). Otaria flavescens (Shaw), South
American sea lion. Mammals in the Seas, FAO, Fisheries.
Series IV, 477–495.
Williams, J.S., White, C.D. & Longstaffe, F.J. (2005). Trophic
level and macronutrient shift effects associated with the
weaning process in the Postclassic Maya. Am. J. Phys.
Anthropol. 128, 781–790.
Worthy, G.A.J. & Lavigne, D.M. (1982). Changes in blood
properties of fasting and feeding harp seal pups, Phoca
groenlandica, after weaning. Can. J. Zool. 60, 586–592.
Yoshida, N. & Miyazaki, N. (1991). Oxygen isotope correlation of cetacean bone phosphate with environmental water.
J. Geophys. Res. 96, 815–820.
Zar, J.H. (1984). Biostatistical analysis. 2nd edn. Englewood
Cliffs: Prentice-Hall.
Journal of Zoology 291 (2013) 119–126 © 2013 The Zoological Society of London